Transmissible Diseases Handbook

VI. Vaccination of Non-Domestic Carnivores : a Review

Joost Philippa, DVM

Institute of Virology, Erasmus MC, Rotterdam, The Netherlands

Since the introduction of vaccinia by Jenner 200 years ago, vaccines have been the first line of defense in controlling infectious diseases in man and domestic animals. Large scale domestic dog vaccination programmes against canine distemper virus (CDV) and canine adenovirus (CAV) became possible in the late 1940’s, when egg-adapted vaccines became available on a commercial basis, followed by tissue culture adapted vaccines in the late 1950’s (Piercy 1961). Before this time these devastating diseases had to be controlled through quarantine and vigilance in capturing feral domestic animals (Dolensek et al. 1977). Historically there have always been two major types of vaccines based on the living state of the antigens. Modified live (MLV) vaccines use attenuated pathogens which reproduce in the vaccinate, thereby elliciting an immunologic response without causing disease (a “controlled” infection). The other major type of vaccine uses antigens that are non-living or inert – killed vaccine (KV). These vaccinations are preferred when safety information is not available, as they do not replicate and are therefore incapable of causing an infection. The proces of inactivation however may be damaging enough to modify immunogenicity, usually resulting in an immune response that is shorter in duration, narrower in antigenic spectrum, weaker in cell-mediated and mucosal immune responses, and possibly less effective in totally preventing viral entry (Murphy et al. 1999). Recent advances in immunology, molecular biology and biochemistry have allowed the construction of subunit vaccines based on viral or bactererial recombinants, peptides, or plasmid vectors, which may lead to safer, more efficacious vaccines that can also be used in exotic species. Vaccines cannot be absolutely guaranteed to provide protection against disease. The principal objective of vaccination is to mimic the protective immune response induced by natural infection, i.e. to elicit a high titre of neutralising antibodies of the appropriate class, IgG and/or IgA, directed against the relevant epitopes on the virion (Murphy et al. 1999). Immunity induced by vaccination or infection in domestic animals has been evaluated mainly by measuring the levels of serum antibodies. The immunologic response that provides protection against infectious agents involves a cellular and a humoral response. For certain infections (e.g. CDV, CAV, canine parvovirus (CPV), feline panleukopenia virus (FPV) or Borrelia burghdorferi ) the humoral responses, although not the only mechanism involved, tend to correlate with level of protection from clinical disease, and therefore may be a useful indicator of the immune status. Other agents (eg, Bordetella bronchiseptica , canine coronavirus (CCoV), feline enteric coronavirus (FCoV), canine parainfluenzavirus (CPIV) and Chlamydia psittaci ) all replicate and cause damage on mucosal surfaces, and might require a mucosal immune response for protection. As a consequence, serum antibody titres do not necessarily correlate with protection (Pfizer 1998). A high concentration of antibodies in an

VI. Vaccination of Non-Domestic Carnivores : a Review animal implies that the animal is probably protected but also could indicate that it may not be possible to stimulate an additional immune response in that animal. Cattle vaccinated with baculovirus-expressed haemaglutinin (H) and fusion (F) proteins of Rinderpest virus (RPV) were not protected against disease caused by challenge exposure despite having detectable antibody titres (Bassiri et al. 1993). For some diseases, caused by persistent intracellular pathogens (viral diseases or intracellular bacteria) the neutralising antibodies and complement may play a less important role than the cellular immunity. Jones et al. (1993, 1997) demonstrated a lack of detectable antibody titre to CDV in ferrets and to peste des petites ruminants (PPRV) in goats after vaccination with a RPV recombinant vaccine based on fowlpox expressing the F and H genes. When these animals were challenged they survived, suggesting that protection against clinical disease may be cell mediated rather than humoral. A comparable study by Fisher et al (2003) using a DNA vaccine showed clear protection after challenge with CDV, with only limited virus neutralising antibody titres. High antibody concentrations do serve to inhibit the spread of virus between cells and thus promote host resistance (Tizard & Ni 1998). Infection with feline rhinotracheitis virus, as all herpesviruses, requires local and cell-mediated immunity, and one study suggests that there is no correlation with protective immunity and antibody titre (Johnson & Povey 1985). Later studies (eg Scott & Geissinger 1999, Dawson et al. 2001) use antibody titres as indicators of protective effect. In general it can be stated that theoretically, cell-mediated immunity is the most effective arm of the immune system in controlling, if not eliminating latent/persistent infections such as those caused by herpesviruses and retroviruses (Murphy et al. 1999). The usefulness of antibody titres to measure immunity is thus limited to only a few disease agents, and in order to obtain a more complete view of the immunologic status of an animal one therefore needs to look at the humoral and cellular responses. One should also keep in mind that an animal that has mounted an immune response after vaccination will possess memory T and B cells, which will remain for years after the antibody titre has declined. These memory cells rapidly differentiate during a subsequent infection into effector cells that can eliminate an infection before clinical signs appear, although the exact mechanism responsible for this longevity is unknown (Ahmed & Gray 1996). One can only know if the measured level of immunity is protective by challenging the vaccinated animal with the pathogen. One of the principal causes of vaccination failures in domestic dogs is maternal antibody interference. MLV vaccines differ in their ability to evade antibodies, and may sometimes be prevented from inducing an immunologic response in the vaccinate when the antibody level is high. The duration of passive immunity is directly correlated with the metabolic size of the animal. Therefore immunoglobulins will persist longer in a larger animal (Armstrong et al. 1942). The “window of vulnerability” during which the pup is vulnerable to infection with virulent virus, but unresponsive to attenuated vaccine virus (Pollock and Carmichael 1990), has been shown to range from 2-5 weeks for parvovirus infection in domestic dogs, but varies between pathogens and vaccinate species. Females close to parturition may be hyperimmunised with an inactivated parvovirus vaccine, so that high levels of maternal antibody delay the window of vulnerability until the offspring are older and better able to withstand the effects of parvovirus infection. The recent debate in veterinary medicine concerning issues related to vaccine efficacy and safety as well as duration of immunity induced by the currently available vaccines (Smith et al. 1995, Schultz et al. 1998, Kruth & Ellis 1998, Tizard & Ni 1998, McCaw et al. 1998, Gumley et al. 1999, Hustead et al. 1999, Twark et al. 2000) has resulted in the need for more objective and scientific data and an increase in research in domestic animals. In non-domestic animals however, there have been only few controlled studies of vaccination (Heerden et al. 1980, Halbrooks et al. 1981, Behlert et al. 1981, Barker et al. 1983, Montali et al. 1983, Green et al. 1984, Bush et al. 1985, Hoover et al. 1985, Paul- Murphy et al. 1985, Briggs et al. 1986, Tham et al. 1987, Follmann et al. 1988, Spencer et al. 1991, 1992, Goodrich et al. 1994, Harrenstien et al. 1995, Schubert et al. 1995, Williams et al. 1996, Henke et al. 1997, Kadoi et al. 1998, Bingham et al. 1999, Harthorn et al. 1999, Pare et al. 1999, Wimsatt et al. 1999, 2003, Maack et al. 2000, Blasco et al. 2001, Federhoff

VI. Vaccination of Non-Domestic Carnivores : a Review et al. 2001, Lambot et al. 2001, Maia et al. 2001, van Heerden et al. 1998, 2002). These are usually restricted to measuring the (humoral) immune response and extrapolating the data from those known in domestic animals, as subjecting (endangered) zoo animals to challenge infections is generally not an option. Challenge studies in dogs have shown a range of reported protective titres – these may differ due to the variety of techniques and standards used. In humans there is a general standardisation of assay methods to measure antibody titres. Non-standardisation of serologic tests makes comparisons between laboratories of questionable use (Luff et al. 1987):

Reported protective titres in domestic dogs : virus protective Reference titre CAV ≥30 Cole et al. 1998 CDV >2 Gillespie et al. 1965; Ackerman & Siebel 1974. ≥20 Gillespie et al. 1958, 1972;Gorham et al. 1966; Prydie 1966; Krakowka et al. 1978; Cooper et al. 1991. ≥24 Jones et al. 1997. ≥30 Gillespie 1966. >50 Olson et al. 1988. ≥96 Mc Caw et al. 1998. ≥100 Appel 1969; Krakowka et al. 1975, Montali et al. 1983; Carmichael et al. 1999.

CPV ≥80 Olson et al. 1988; Carmichael et al. 1983, 1994, 1997; Appel et al. 1979; Pollock and Carmichael 1982; Meunier et al. 1985. RV ≥20 Bunn et al. 1984

Twark et al. (2000) report that CDV titres above 5 are indicative of an adequate antibody response in domestic dogs, although level of protection is unknown, and recommend CDV revaccination when titres are below 32. Carmichael et al. (1983) demonstrated that dogs with a CPV titre below 100 were not protected. Titres of 200-800 were protective in some dogs, titres above 1600 appeared to be protective in all dogs. There is still no general consensus on how often domestic animals need to be revaccinated - for most vaccines there is little information on the duration of immunity. It is, however, recognised that protective immunity to CDV following MLV vaccination is of long duration, perhaps even lifelong. For other viruses or components of combination vaccines this duration may not be of such long duration. Vaccines used in domestic animals are approved for use in specific animals under specific conditions, and any other use is therefore extra-label. Most of the vaccines are not approved for non-domestic species, therefore there is always a potential liability to such use (Bittle 1993). MLV vaccines have been designed to be minimally virulent, while retaining maximal immunogenicity in their domestic counterparts. When used in other species or delivered by another route the residual virulence may cause disease (Tizard et al. 1990). It is not unusual to observe side-effects such as elevated temperature, swelling, and irritation at the site of injection, or systemic anaphylactic reactions like hyperaemia, hypersalivation, or vomiting (Greenacre 2003) that may in some cases be severe (Karesh et al. 1983). Several viruses induce a supression of the immune system, and it is known that some attenuated virus strains may still be able to cause immunosuppression, e.g. MLV CPV (Krakowka et al 1982). Sometimes the individual vaccine strains are not detectably immunosuppressive, but when combined in a combination vaccine they may induce a suppression of blood lymphocyte counts (Phillips et al. 1989a). Enhanced virulence of canine

VI. Vaccination of Non-Domestic Carnivores : a Review distemper virus produced in canine cell-cultures has been reported when used in combination with CAV-1 and live CCV vaccines (Carmichael et al. 1983, Martin et al. 1985, Wilson et al. 1986), and may lead to encephalitis.

There are many examples of vaccine-induced disease: virus Species reference CAV Domestic dog ( Canis familiaris ) Appel et al. 1978. Maned wolf(Chrysocyon brachyurus ) Thomas-Baker et al. 1985. CDV Domestic ferret ( Mustela putorius AVMA 1966; Wimsatt et al. 2001. furo ) Kinkajous ( Potus flavus ) Kazacos et al. 1981. Red panda ( Ailurus fulgens ) Bush et al. 1976; Itakura et al. 1979. Black-footed ferrets ( Mustela Carpenter et al. 1976; Pearson et al. nigripes ) 1977. African wild dogs ( Lycaon pictus ): Mc Cormick et al. 1983; Montali et al. 1983; Durchfeld et al. 1990. Maned wolf Thomas-Baker et al. 1985. Bush dog ( Speothos venaticus ) Mc Innes et al. 1992. European mink ( Mustela lutreola ) Sutherland-Smith et al. 1997. Ek-Kommonen et al. 2003 Gray fox ( Urocyon inereoargenteus ) Halbrooks et al. 1981. Fennec fox ( Fennecus zerda ) Mehren et al. 1984. RV Domestic dog Pedersen et al. 1978; Whetstone et al. 1984. Domestic cat Erlewein et al. 1981. Skunk ( Mephitis mephitis ) Debbie et al. 1979. Raccoon ( Procyon lotor ) 1978. FeLV Cheetah Briggs et al. 1986. FHV Domestic cats North et al. 1978 Pallas cat Wallach & Boever 1983 FPV Felidae: Behlert et al. 1981 Cheetah ( Acinonyx jubatus ) Crawshaw et al. 1996

Preventive medicine is especially important in the management of non-domestic animals for several reasons: the ability to mask or hide illness or distress as a means of survival means that by the time signs of disease are exhibited, the underlying disease condition may have advanced to a critical stage. Another reason is that the use of anaesthesia is required to perform a proper physical examination. Active immunisation is only one of the factors (eg nutrition, parasite control, hygiene) associated with preventive medicine. Recommendations for use in exotic mammals are generally based on tradition, anecdotal/personal experiences or taken from limited precise, published data. This has led to a plethora of differing opinions and therefore the use of many different protocols in zoological collections. In general, inactivated viral or bacterial vaccines are preferred for use in exotic animals. The type, serial number, and source of product should be recorded in the medical records (Joslin et al. 1990). Use of polyvalent vaccines containing unnecessary antigen (one the species is not susceptible to) should be avoided where possible. Animals with active clinical illness should not be vaccinated. In the event of a viral disease outbreak in an animal collection, all susceptible species should be vaccinated immediately and boostered 10-14 days later, regardless of age and last time of immunization (Phillips 1989). Some drugs, such as tetracycline, chloramphenicol, dapsone, clindamycin, griseofulvin, nalidixic acid and sulphamethoxypyradizine have been associated with an inadequate response to vaccination (Kruth – Ellis 1998). Vaccination should also be avoided in animals undergoing glucocorticoid therapy, although challenge studies have been performed which show that “immuno-

VI. Vaccination of Non-Domestic Carnivores : a Review suppressive” doses given at the time of vaccination do not significantly affect the level of post-vaccinial immunity to canine distemper or rabies (Dhein et al. 1986). When using remote delivery systems one must be sure that a full dose has been delivered. Syringe darts may rebound quickly on impact and fail to deliver the dose required to elicit a satisfactory immune response (Aiello 1998). Any vaccination programme should also take the current local prevalence of the pathogen into account, upon which the decision can be made if vaccination is warranted.

Disease susceptibility CAV CDV FPV FeLV FHV FCa Rabie Lepto Toxo V s Canidae + + - - - - + + + Felidae - + ++ + + + + + ++ Ursidae + + + - - - + + + Procyonidae - + + - - - + + + Mustelidae - + + - - - + + + Viverridae - + + - - - + + ? Hyanidae + + + - - - + + ? Pinnipedia + + - - - - + + +

Canine distemper virus (CDV) : All families of the order Carnivora are susceptible to CDV, and it is among the most significant infections of many species. Christensen (1963) recommended vaccination against CDV in susceptible zoo animals, with the addition that vaccination of young animals at an earlier stage than in dogs is preferred. CDV vaccination is recommended in all members of the Canidae, Procyonidae and Mustelidae by all authors. There is no mention of vaccination of felids against CDV in literature until several outbreaks occurred among large cats in zoos and the wild (Fix et al. 1989, Appel et al. 1994, Munson et al. 1995, Wood et al. 1995, Roelke-Parker et al. 1996, Meehan et al. 1998, Cameron et al. 1998, Miller & Anderson 2000). Following this, the vaccination of large cats is mentioned as being possible, but not recommended – unless in high risk situations - as risk of exposure is generally low, and vaccination carries some risk (Junge et al. 1995, Kennedy-Stosskopf 1996, Aiello 1998, Miller & Anderson 2000, Woodford 2001, www.5tigers.org). The susceptibility of members of the Ursidae and Hyaenidae to canine distemper virus is deemed questionable by some authors, and therefore not recommended by these authors (Fraser 1991, Aiello 1998). Although clinical disease as a result of CDV infection is rare in ursids (Poston & England 1992), serologic surveys have shown the presence of CDV specific antibodies (Munson et al. 1995, Marsilio 1997, Dunbar et al. 1998, Maack et al. 2000). Clinical disease and presence of CDV specific antibodies has been documented in spotted hyaenas ( Crocuta crocuta ) (Montali et al. 1987, Alexander et al. 1995, Haas et al. 1996, Harrison et al. 2002) and a palm civet ( Paguma larvata ) (Machida et al. 1992), therefore vaccination is recommended in these species by other authors (Fowler 1986, Phillips 1989, Miller 1989, Burroughs 1992, Junge 1995, Woodford 2001). Miller & Anderson (2000) recommend vaccination of Viverridae , do not recommend vaccination of Ursidae , and omit Hyanidae from their article. In general, when vaccination is recommended, the same regime is used in the different families. Due to the possibility of immunosuppressive effects of multivalent vaccines, it is recommended that the distemper vaccine be given separately at a reasonable interval from the other components (Montali et al. 1994) A problem faced in the prophylaxis of distemper in exotic carnivores is the variation between and within species in their reaction to MLV vaccines, with possible lethal consequences. There are two distinct types of MLV CDV vaccine, one produced in avian cells and the other in canine kidney cells, and neither is safe for use in all potential target species. Chicken embryo-adapted live virus distemper vaccines attenuated for ferrets have protected them from challenge with an infective dose of virulent virus within 48 hours after vaccination (Baker et al. 1952). Fromm D (Solvay Animal Health Inc.) appeared to be safe

VI. Vaccination of Non-Domestic Carnivores : a Review and efficacious for use in maned wolves, bush dogs and fennec foxes (Montali et al. 1983). But avian cell vaccines have caused disease in mink, ferrets and foxes (Sutherland-Smith et al. 1997, Carpenter et al. 1976, Henke et al. 1997). Fervac-D, also of avian origin caused fatal disease in 1 of 8 red pandas (Montali et al. 1994). Vaccine of canine origin has been responsible for vaccine induced distemper in a large number of species (see table ). Non- domestic canine pups can be vaccinated with a MLV measles vaccine (Klös & Lang 1982, Frankenhuis & Visee 1985) - measles and canine distemper virus are antigenically closely related, and the measles virus is not neutralised by the maternal antibodies in 6 week old puppies of domestic dogs (Appel et al. 1984). The second and all subsequent vaccinations should be with a MLV CDV vaccine. Until 1983 the use of MLV is mentioned without warning (Klös & Lang 1982, Wallach & Boever 1983, Miller 1989). After this KV are recommended for use in exotic species (Fowler 1986, Gabrisch & Zwart 1987, Franke et al. 1989, Fraser 1991, Aiello 1998) even though the efficacy of KV has been questioned (Appel et al. 1984, Sikarski et al. 1991). Currently there are no killed CDV vaccines commercially available, because there is no demand for its use in domestic dogs, and the market for zoo animals is too small (Appel & Montali 1994). Between the different commercially available MLV vaccines there is a clear difference in vaccine efficacy, as has been demonstrated in domestic dogs (Appel et al. 1987, Rikula et al. 1996, Kommonen et al. 1997). Considering the high incidence of vaccine induced disease, Miller & Anderson (2000) mention that in some cases strict isolation may be preferable to vaccination. The large range of (highly susceptible) host species in zoos for which vaccination is recommended underpins the need for the production of a safe and efficacious vaccine. An experimental subunit vaccine incorporating the CDV F and H proteins into immuno stimulating complexes (ISCOM) has been developed for use in dogs and seals (de Vries et al. 1988, Visser et al. 1992), and proved to be capable of producing humoral and cellular immunity. Although the immunity achieved was not sterile (infection of the upper respiratory tract occurred), the vaccinated seals were protected from a potentially lethal challenge with phocid distemper virus (Visser et al. 1992). The ISCOM vaccine has since been used experimentally in several European zoos (Schaftenaar pers. comm), and its potential use in non-domestic felids has been proposed in special cases (Kennedy-Stoskopf 1996). An experimental adjuvanted killed CD vaccine produced by M.J.G. Appel has been used in red pandas and giant pandas in several zoos. The vaccine appeared to be safe and effacacious, but produced low titres with inadequate durability, requiring booster vaccinations two to three times annually (Montali et al. 1994). This vaccine is no longer produced. In Germany a small amount of inactivated vaccine is produced for use in zoos (Geyer and Matern pers. comm. 2001). In 1997 a recombinant virus vectored CDV vaccine was introduced (Stephenson et al. 1997) and tested for its safety and efficacy along with MLV components (Pardo et al. 1997). Following vaccination experiments in mice using a vaccine expressing the H and F protein in mice, a vaccine containing the H, F and nucleocapsid (N) constructs produced highly encouraging results in domestic dogs after challenge with virulent virus, although the mechanism of protection was not clear (Cherpillod et al. 2000). Recently a monovalent canarypox-vectored vaccine expressing the H and F surface antigens of CDV has become commercially available in the US, and its efficacy and safety in domestic ferrets has been demonstrated (Wimsatt et al. 2001). In black-footed ferrets ( Mustela nigripes ) x Siberian polecat ( Mustela eversmanni) hybrids the use of this vaccine has produced a good immune response (Williams & Montali 1998), and has since been used and evaluated in a large number of exotic species (Montali pers. comm.). This vaccine, Purevax (Merial) is registered for use in domestic ferrets, but its off-label use in all susceptible species in zoos is recommended by the American Association for Zoo Veterinarians (AAZV) and Woodford (2001). In the European Union its use is not permitted. The main advantage of avipox- vectored vaccines is their safety, the foreign genes in the vector are expressed, inducing protective cellular and humoral immunity in the absence of the complete virus, and therefore eliminating the possibility of infection. Members of the Avipox genus are distinguished by their host restriction to avian species, eliminating the potential for dissemination of the vector

VI. Vaccination of Non-Domestic Carnivores : a Review within the vaccinate and therefore the spread of the vector to nonvaccinated contacts or the environment (Paoletti 1996). Virus replication is blocked at a late stage of morphogenesis in mammalian cells, importantly leaving the synthesis of viral proteins unimpaired (Sutter & Moss 1992). For unknown reasons, canarypox virus appears to be superior to fowlpox virus in the induction of immune responses in mammals (Moss 1996). Recent research has shown that replication-competent CAV-2 recombinant vaccines expressing the H and F antigens of CDV triggered both a significant seroconversion and protective immunity in puppies born to CDV and CAV-2 immune dams, thereby overcoming the passive immunity (Fischer 2002).

CDV Vaccination regime recommended in domestic dogs: • Initial at 6 weeks, repeat every 2 weeks until 12 weeks. Booster annually with MLV vaccine (Appel et al. 1999, Carmichael 1999, Dodds et al. 1999).

CDV vaccination Regimes recommended for use in non-domestic species species vaccine regime booster reference All MLV Initial at 3-6 weeks, at 9 weeks biannually Klös & Lang 1982 susceptible combination vaccine. Single vaccination after 12 weeks Mustelidae MLV 10 weeks * Klös & Lang 1982 All KV or MLV Initial at 5-6 weeks repeat every 2 weeks annually Wallach & Boever susceptible until 15 weeks 1985 Mustelidae KV for Initial at 8 weeks, repeat after 2-3 weeks * Wallach & Boever blackfoot & 1985 initial Procyonida KV Initial at 6-8 weeks, repeat every 2-3 annually Wallach & Boever e weeks until 14 weeks 1985 All Initial at 8 weeks, repeat after 2-3 weeks annually in affected areas, Frankenhuis & Visee susceptible otherwise every 2-3 years 1985 All KV Initial distemper/measles at 6-8 weeks, at annually Burroughs 1992 susceptible (unavailable) 12-14 weeks combination vaccine. Procyonida Initial at 8 weeks, repeat at 12 and 16 or * Paré et al. 1999 e 18 weeks of age All Single dose after weaning im, monthly annually Fraser 1991, Aiello susceptible booster up to 4 months 1998 All Initial at 6-8 weeks, repeat every 2-3 annually Phillips 1989, Cubas susceptible weeks with a total of 3 vaccinations, in et al. 1996 special cases (ie early weaning, ill juveniles, high probability of exposure to disease) extended to 4 or 5. All ISCOM or 8, 11, 14 weeks of age annually Blijdorp, Rotterdam susceptible KV Zoo, (unavailable)

Parvovirus infections: Infections with Feline Panleukopeniavirus (FPV) have been reported in captive felids since the 1930’s (Hindle & Findlay 1932, Goss et al. 1942), and have since been reported in a large number of feline species. All members of the Canidae, Felidae, Viverridae , Mustelidae (except for the domestic ferret, Parrish et al. 1987), Procyonidae and Ursidae are susceptible and vaccination is recommended. Although there is some difference of opinion on the susceptibility of Hyaenidae , vaccination is recommended (Junge 1995). Vaccination regimes reported by these authors are as those for the exotic cats. In 1947 a new viral gastroenteritis was observed in farmed mink ( Mustela vison ) in Canada (Schofield 1949). That virus, closely related biochemically and serologically to FPV, was later named mink viral enteritis, and currently probably occurs wherever mink are farmed (Pollock and Larsen 1990). In 1978 a virus infecting canine species emerged with clinical similarities to FPV infection in cats (Appel 1979). This virus, referred to as canine parvovirus type 2 (CPV- 2) is closely antigenically and pathogenically related to FPV. Members of the Canidae, Mustelidae, Viverridae and Procyonidae are considered to be susceptible, but the virus has not got the ability to replicate in Felidae . In 1979 and around 1984 new antigenic types of CPV (CPV-2a and CPV-2b) emerged with an increased host range including both domestic and large cats (Steinel et al. 2000), although the large cats appear to have a higher susceptibility for these virus types (Steinel et al. 2001). For all susceptible species

VI. Vaccination of Non-Domestic Carnivores : a Review vaccination is recommended (Fraser 1991, Aiello 1998, Steinel et al. 2001). Other authors recommend vaccination of canidae only (Wallach & Boever 1985, Cubas et al. 1996). Canidae may be vaccinated with a FPV vaccine, and Felidae may be vaccinated with CPV vaccine due to the close antigenic relationship (Pollock & Carmichael 1983). In general, when vaccinating non-domestic species, the vaccine selected should be based on the similarity of the hosts (e.g. CPV in coyotes) or the known or probable virus susceptibility of the host to be vaccinated (e.g. FPV vaccine in raccoons) (Barker and Parrish 2001). It is recommended to vaccinate members of the Canidae with CPV-2 vaccines, and considering the high incidence of infections with CPV-2a and CPV-2b in large cats an inactivated vaccine containing these types rather than CPV-2 would be desirable, but is not yet commercially available. There is debate over vaccine dose in relation to size of species, and the use of KV and MLV vaccines. Povey and Davis (1977) suggest that it is probably unnecessary to increase the dose or antigen mass when using KV in large species, due to the antigenic efficiency of parvoviruses and the use of adjuvants. Increased or double doses have been recommended for the vaccination of large cats >50 kg, which will subsequently develop higher antibody titres (Fowler 1977, Wallach - Boever 1983, Fraser 1991, Aiello 1998). In other studies antibody titre does not appear to be dose dependent (Wack 1991), large felids do not require larger doses than the 1ml dose used in domestic cats to develop protective titres (Bush et al. 1981). MLV vaccines probably overcome the consideration of animal size in relation to dose of vaccine (Povey and Davis 1977), although the increased potency may result in decreased safety. Some MLV vaccines reported to be safe for one species may be insufficiently attenuated for use in another species, and have caused vaccine-induced disease (Klös & Lang 1982, Wallach & Boever 1983, Frankenhuis & Visee 1985, Appel et al., Fraser 1991, Aiello 1998, Woodford 2001). Christensen (1963) reported abortive cases of depression and diarrhoea with recovery after 1 or 2 days’ symptoms following the introduction of systematic FPV vaccination. Visee (pers. comm. 1974 & 1975) reported clinical panleukopenia in 3 vaccinated Siberian tigers and 1 leopard ( panthera pardus ), of which 2 fatal. Therefore the use of KV is generally recommended in exotic species, although the production of antibodies is not as effective and the duration of immunity is shorter. KV FPV vaccine used in bush dogs (Speothos venaticus ) did not protect them from infection – protective titres were not reached before 23 weeks of age during which period they were susceptible to infection (Janssen et al. 1982). Fowler (1977) reports that MLV vaccines have been used in different wild felid species, and are apparently safe. Many authors after this recommend the use of the highly antigenic KV vaccine (Klös & Lang 1982, Wallach & Boever 1983, Appel et al., Fraser 1991, Aiello 1999), or at least KV for the initial vaccinations which can then be boostered with MLV (Frankenhuis & Visee 1985, Fowler 1986, Gabrisch & Zwart 1987). Phillips (1989) recommends the use of KV without components for the feline respiratory viruses in mustelidea, procyonidae and viverridae. MLV vaccine should never be used in in pregnant felidae, foetal infection results in cerebellar hypoplasia with clinical ataxia in the kitten (Fowler 1986). Many different regimes have been tried, in which the timing of the initial vaccination is one of the main variables. Interference with primary immunisation by maternal antibodies is the commonest cause of “vaccine failure” in both domestic (Greene 1990) and non-domestic carnivores (Janssen et. al. 1982; Wack et al. 1993). Vissee (pers. com. 1975) reorted that after a change in the vaccination regime (6, 12, 26 weeks to 12, 16, 20 weeks) no clinical signs were reported following MLV vaccination, suggesting that maternal antibodies interfere with vaccination during the first 3 months. No controlled studies on the half-life of maternal antibodies to FPV in non-domestic species have been performed, and it should not be directly extrapolated from the 9.5 days determined in domestic cats (Scott 1970). Therefore the vaccination recommendations for non-domestic species are the same as those used in domestic species during maternal immunity. Combination vaccines containing MLV CDV, CAV-2, CPI-3, and FPV/CPV have been used in wild canidae without adverse effects, but with variable results, especially among non- canine species. Burroughs (1992) recommends its use in canidae, viverridae and hyaenidae.

VI. Vaccination of Non-Domestic Carnivores : a Review

A multivalent KV vaccine (Fel-O-Vax PCT, Fort Dodge Lab Inc.) provides good antibody titres to the three major infectious viral diseases of domestic cats (panleukopenia, rhinotracheitis and calicivirus). The European Endangered Species Program (EEP) recommends 1 ml of Fel-O-Vax be used for boosters in adults; juveniles should be vaccinated at 8, 12, and 16 weeks, repeated at 6 months, and then given annual boosters. This is the same schedule used in domestic cats. Another regime recommended is repeated vaccinations with 2 week intervals for 3 injections or until 16 weeks of age (Woodford 2001). When cheetah cubs are vaccinated every 4 weeks from 8-16 weeks they may not develop and maintain protective antibody titres during their first year of life. When these cubs are vaccinated every 2 weeks from 8-16 weeks will develop protective titres. A booster may need to be given at the age of 40 weeks to insure that titres are maintained during the first year of life. There is much individual variation – boosters every 3 months may be warranted in high risk situations (Wack et al. 1993) - but a single annual vaccination may be adequate to maintain protective antibody titres (Wack 1991).

FPV vaccination recommendation in domestic cats : • 8, 12, 16 weeks, booster at 6 months, then annually (Fel-O-Vax, Fort Dodge)

FPV vaccination Regimes recommended for use in non-domestic species species vaccine regime booster reference All susceptible MLV 6, 12, 26 weeks Visee pers comm 1974 All susceptible MLV or KV 12, 16, 20 weeks Visee pers comm 1975 All susceptible KV or MLV 4, 8, 12, 16 weeks annually when using KV Fowler 1977 All susceptible 4, 8, 16 weeks (bi-)annually Klös & Lang 1982 All susceptible 6-8 weeks, repeat every 2-3 weeks until 14 annually Wallach & Boever weeks of age 1983 All susceptible 1-2 doses KV, then after 3 weeks MLV. annually in affected areas, Frankenhuis & MLV at 8, 11 weeks. otherwise every 3 years Visee 1985 All susceptible KV 2, 4, 8, 12, 16 weeks (colostrum deprived). annually (KV or MLV) Fowler 1986 8, 12, 16 weeks (naturally weaned) All susceptible 3 x KV with 2 weeks interval, then 2 x MLV (bi-)annually Gabrisch & Zwart with 4 weeks interval (colostrum deprived), 1987 3 x MLV with 3-4 weeks interval starting at 7-8 weeks. Skunks Initial at 8-10 weeks, repeat after 3 weeks Gabrisch & Zwart 1987 All susceptible pregnant females should be boosted annually Sacramento zoo during gestation 1990 Felidae KV, Initial KV at 3 months, MLV combination annually (unavailable) vaccine at 4 months All susceptible Initial at weaning and repeated at least annually Junge 1995 twice with 2 week intervals All susceptible 8 and 12 weeks annually Meltzer et al. 1996 All susceptible 2 x with 2 weeks interval 6-12 months Fraser 1991, Aiello 1998 All susceptible KV 8, 10, 12, 14, 16 weeks, repeat at 6 annually Miller & Anderson months 2000 All susceptible KV 8, 11, 14 weeks annually Blijdorp, Rotterdam Zoo

CPV vaccination Regimes recommended for use in non-domestic species species vaccine regime booster reference All susceptible Initial at 8-12 weeks, 2 nd vaccination 3 weeks annually, every 6 months Wallach & Boever later in endemic areas 1985 All susceptible As in domestic dogs Frankenhuis & Visee, 1985 All susceptible MLV Initial at 3 months annually Burroughs 1992 All susceptible Initial at 8 weeks, repeat 3-4 times with 2-3 Cubas et al. 1996 week intervals All susceptible 8, 11, 14 weeks annually Blijdorp, Rotterdam Zoo

VI. Vaccination of Non-Domestic Carnivores : a Review

Infectious canine hepatitis / Canine Adenovirus-1 (CAV-1) : Canidae, Ursidae and Mustelidae are susceptible to canine adenoviruses (Mann et al. 1980, Whetstone et al. 1988). Annual vaccination of Ursidae is recommended by some authors (Sacramento zoo 1990, Fraser 1991, Aiello 1998), depending on risk of exposure (Fowler 1986, Appel 1987) or not at all (Wallach & Boever 1983, Frankenhuis & Visee 1985, Junge et al. 1995, Miller & Anderson 2000). Burroughs (1992) recommends vaccination of Canidae and Hyaenidae . KV has been recommended for use in genera other than Canidae , as MLV may prove virulent (Klös & Lang 1982, Appel 1987). Currently there is no KV commercially available. The diluent portion of Adenomune-7 however, contains a killed CAV-2 antigen that may be used in highly susceptible species like maned wolves (Woodford 2001). Commercial combination vaccines that include CDV and MLV CAV-1 or CAV-2 are generally used. CAV-1 is the causative agent of of infectious canine hepatitis, CAV-2 is the causative agent of respiratory disease. The two viruses are closely antigenically related, and vaccination with CAV-2 provides cross- protection against CAV-1 without causing adverse postvaccinial reactions like corneal opacity, common in domestic dogs after vaccination with MLV CAV-1, and reported in maned wolves by Thomas-Baker et al. (1985). Although clinically dramatic, the oedema usually resolves after a few days without consequence. Another reason was the diminition of postvaccinial encephalitis which was noted after subtitution of CAV-2 for CAV-1 in combination vaccines (Carmichael 1999).

CAV vaccination Regimes recommended for use in non-domestic species species vaccine regime booster reference All susceptible Initial at 3-6 weeks bi-annually Klös & Lang 1982 All susceptible MLV or KV Initial at 11-12 weeks, repeat after 2- Annual Wallach & Boever 3 weeks 1983 All susceptible As in domestig dogs Frankenhuis & Visee 1985 All susceptible MLV (caution) KV As in domestic dogs annually or prior to Appel 1987 possible exposure All susceptible CAV-2 MLV Initial at weaning, monthly booster annually Fraser 1991, Aiello up to 4 months of age 1998 Alls usceptible MLV combination Initial at 3 months annually Burroughs 1992

Herpesvirus infections : All smaller exotic Felidae are susceptible to feline herpesvirus (FHV), larger Felidae have no or mild symptoms. Vaccinations currently available are KV or MLV, but KV is recommended. Vaccines commercially available (eg Fel-O-Vax) are usually in combination with other agents (eg FPV, FCaV, Chlamydia). Humoral titres are usually short-lived and boosters every 3 months may be required in high-risk situations (Wack et al. 1993). Klös and Lang (1982) recommended vaccination of Mustelidae and Viverridae , all other authors regard Felidae as the only susceptible animals. Fatal phocine herpesvirus type 1 (PhHV-1) infections have been reported in young and immunocompromised harbour seals in rehabilitation centres (Osterhaus et al. 1985, Borst et al. 1986, Gulland et al. 1997, Harder et al. 1997). An experimental sub-unit vaccine using the gB protein of PhHV-1 has been produced that proved to be safe and provided protective immunogenicity after challenge infection in domestic cats. Humoral and cellular immunogenicity was produced in harbour seals (Martina et al. 2001; 2003).

VI. Vaccination of Non-Domestic Carnivores : a Review

FHV vaccination Regimes recommended for use in non-domestic species species vaccine regime booster reference All susceptible Initial at 9 weeks, repeat after 3 weeks. after 6 months Klös & Lang 1982 Adult cat twice with 2-3 weeks interval Felidae MLV Initial at 8 weeks, repeat every 3-4 annually, in high incident Wallach & Boever weeks until 14 weeks of age areas every 6 months 1983 Felidae As in domestic cats Frankenhuis & Visee 1985 Felidae MLV Naturally weaned: Initial at 7-8 weeks, annually, endangered Gabrisch & Zwart repeat 3 times with 3-4 weeks interval. cats and cheetahs every 1987 Not naturally weaned: Initial at 7-8 6-9 months. With weeks, repeat 2 times with 3-4 weeks KV booster, larger cats interval. need 2-5 x dose Felidae MLV Pregnant female should be boosted annually Sacramento Zoo 1990 Felidae KV or MLV Single dose at weaning. Monthly annually Fraser 1991, Aiello combination intervals until 4 months of age 1998 All susceptible combination Repeat at 2 week intervals for 3 annually Woodford 2001 KV injections or 16 weeks of age All susceptible KV 8, 11, 14 weeks annually Blijdorp, Rotterdam Zoo

Feline Leukemia virus (FeLV) : Has been reported in exotic felids, and efficacy of a subunit vaccine has been demonstrated (Briggs et al. 1986, Citino ety al. 1988, Pettan et al. 1992). It is recommended to serologically test all Felidae for exposure. In 1986 vaccination with the then recently developed Leucocell vaccine was recommended by Gabrisch & Zwart. Due to the low prevalence in exotic cats, and the interference with serologic antibody screening, vaccination is not generally done (Citino et al. 1988, Phillips 1989, Junge et al. 1995, Kennedy-Stosskopf 1996), but may be done when there is close contact with feral cats (Miller & Anderson 2000).

Leptospirosis : Canidae, Procyonidae, Ursidae, Mustelidae , and Pinnipedia are susceptible (Shotts 1981). A recent study in Rio de Janeiro Zoo, Brazil revealed an antibody prevalence of 37.7% of all animals tested – carnivores and non-carnivores - belonging to 10 families, out of which seroprevalence was most common in Canidae and Procyonidae (Lilenbaum et al. 2002). Raccoons, opossums, and rodents can act as reservoirs and concurrently transmit infection to zoo animals. Vaccination is highly serovar specific: the carnivores should be vaccinated with bacterins that contain immunogens against Leptospira interrogans serovar canicola and icterohaemorrhagiae. Vaccinations may influence the immune response in young animals - vaccination of pups younger than 9-10 weeks of age is not recommended (Appel et al. 1999). Vaccination does not necessarily prevent shedding of the organism (Aiello 1998).

Leptospirosis vaccination Regimes recommended for use in non-domestic species species vaccine regime booster reference Canidae Initial at 12 weeks, repeat after 2-3 weeks annually Wallach & Boever 1983 Procyonidae Initial at 12-14 weeks annually Wallach & Boever 1985 / Mustelidae All As in domestic dogs Frankenhuis & Visee susceptible 1985 Ursidae Initial at 8 weeks, repeat at 12 and 16 weeks of annually Sacramento zoo 1990 age All annually Junge et al. 1995 susceptible All 1-2 ml dose im or sc at 6-8 weeks, repeat after Bi-annual Fraser 1991, Aiello susceptible 2 weeks 1998 Canidae/ Bi-annual Woodford 2001 Procyonidae

VI. Vaccination of Non-Domestic Carnivores : a Review

Rabies : All mammal species are susceptible. Previously rabies vaccination was recommended in all circumstances (Klös & Lang 1982, Wallach & Boever 1983, Fowler 1986, Appel 1987). More recently recommendations are to vaccinate depending on location, risk of exposure, or possible outbreak (Fraser 1991, Junge et al. 1995, Aiello 1998). In areas where the incidence of rabies in local wildlife (skunks, raccoons, foxes) is high, vaccination is recommended. Local veterinary authorities should be conctacted regarding the legal aspects of extra-label vaccination, as some areas may have restrictions. Klös & Lang (1982) recommended use of MLV, except for younger animals. All other authors agree that non- domestic animals should be vaccinated with KV only. MLV vaccines have not been available commercially after rare occasions where the vaccine caused rabies-like disease in dogs. The efficacy of KV vaccines were questioned by Fowler (1986), but a KV vaccine (Imrab, Pitman Moore) has proven to be efficacious and safe, and been approved for use in domestic ferrets (Rupprecht et al. 1990). A great reduction in wildlife rabies has been accomplished by oral immunization (see below).

RV vaccination Regimes recommended for use in non-domestic species species vaccine regime booster reference All KV Initial at 4-6 months annually Wallach & Boever susceptible 1983; Junge et al. 1995 Felidae KV Initial at 6 months annually Wallach & Boever 1983 All KV Initial at 6 months annually Sacramento zoo 1990 susceptible All KV Initial at 3-4 months annually Fraser 1991, Aiello susceptible 1998 All Initial at 3-6 months tri-annually, during Burroughs 1992 susceptible outbreak more often

Toxoplasmosis : Many species of zoo mammals (but also birds) are highly susceptible to Toxoplasma Gondii infections, especially New World monkeys and marsupials, although members of the Felidae family are the definitive host, and the only animals that pass the oocyst in the faeces. This protozoan parasite has been reported in several species of non- domestic felidae, of which the Pallas cat appears to be highly susceptible (Dubey et al. 1988, Dorny et al. 1989, Ocholi et al. 1989, Swanson et al. 1999, Silva et al. 2001). There are a number of different vaccines, of which New Zealand S48 vaccine containing live tachyzoites, proved to be capable of inducing acute, fatal toxoplasmosis and is therefore considered to be unsuitable for use in macropods (Lynch et al. 1993). An alternate study suggested that oral vaccination with Hammondia Hammondi oocysts – a closely related non-pathogenic protozoan - may offer partial protection to the clinical effects, but does not prevent infection by T. gondii (Reddacliff et al. 1993). Recently an experimental recombinant FHV vaccine expressing the ROP2 antigen of T.gondii has been developed and proven efficacious in domestic cats (Mishima et al. 2002), but this is not yet commercially available.

Vaccination of free-ranging wildlife:

Should free-ranging wildlife be vaccinated? It is an interference of the natural selection, and therefore a topic under discussion. Re-introduced or translocated animals will not have been challenged under natural conditions with the local pathogens when young (and maternal immunity is still present), and therefore need to be vaccinated to obtain a level of immunity against these pathogens. Recently IUCN guidelines for the reintroduction of captive animals into the wild have been published (Woodford 2001). Pre-release vaccination of animals to be rehabilitated or translocated should be considered by the veterinarian after evaluating the immunological status, and the risk of infection upon release into the destined area.

VI. Vaccination of Non-Domestic Carnivores : a Review

When vaccinating wildlife it is of utmost importance to consider the fact that MLV vaccines may not be sufficiently attenuated for exotic species, and that vaccine induced disease or shedding of virulent virus may occur, thereby infecting free-living populations. Another problem faced is the difficulty to booster under field conditions, so that the level of immunity may not be sufficient. It is therefore recommended to complete the vaccination regime before release when possible. When this vaccination is carried out during the “preparation stage”, sufficient time is allowed to develop the required immunity and detect possible adverse effects. Following the phocine distemper (PDV) epidemic of 1988 (Osterhaus et al. 1988, Osterhaus & Vedder 1988, Kennedy et al. 1988) and the development of an experimental ISCOM (Osterhaus et al. 1989, Visser et al. 1992), all rehabilitated seals from the rehabilitation and research centre Pieterburen have been vaccinated before release. The duration of protective immunogenicity following this vaccination is unknown, and is intended to last for the duration of stay in the rehabilitation centre. The discussion of whether to start vaccinating the wild population flared up during the recent PDV epidemic of 2002, but was not considered a viable option (Trilateral seal expert meeting 2002, DEFRA 2002). Vaccination of seals with a MLV vaccine is contraindicated (Kennedy et al. 2001). Vaccination of endangered species to infectious diseases may aid in the survival of these species. African wild dog (Visee et al. 2001) and black-footed ferret (Williams & Thorne 1999) conservation projects have been severely affected by CDV outbreaks, and much work is done on the production of a safe and efficacious vaccine (Montali et al. 1998, Visee 2001, van de Bildt et al. 2002). Vaccination of a wild population of Mediterranean monk seals ( Monachus monachus ) was considered during a morbillivirus epizootic in the mediterranean in 1992 (Osterhaus et al. 1992). During the PDV outbreak among Northern European Harbour seals in the summer of 2002, vaccination was also considered in the UK, but not deemed feasible (DEFRA 2002). The zoonotic and economic aspects of rabies infection have resulted in prophylactic immunization of domestic dogs and the eradication of canine rabies in several countries (Bögel 1982). Following this achievement attention was focused on free-ranging vector species, which were much more difficult to vaccinate. The development of a MLV vaccine which vaccinated foxes by the oral route (Baer 1971) was a major step in the right direction, which proved its value when an advancing epidemic was stopped by the vaccination zone (Steck et al. 1982). This vaccine has since been replaced by a vaccinia recombinant vaccine (Pastoret 1997), which has proven to be efficacious, and safe for the target species, the fox, as well as for numerous non-target species (Black et al 1993). To be effective the vaccine must be brought into contact with oral and /or pharyngeal mucosa in a sufficient number of target animals via bait. Factors affecting uptake: size, texture, shape of bait and vaccine container, as well as physical and chemical characteristics. One should take into account bait density, distribution method (manual, aerial or both), sequence and frequency of bait distribution, season, selection of specific baiting areas, strategies for expansion of baiting areas and the overall duration of vaccination campaigns (Rupprecht et al. 2001). Research is being conducted on the development of ideal baits and baiting systems for different species (Steelman et al 1998, Knobel et al 2002, Linhart et al 2002). Oral vaccination may be used in the eradication of other diseases of wildlife in the future. Wimsatt (1999) reported potential oral efficacy of an experimental canarypox vectored recombinant CDV vaccine in a preliminary study, and this oral efficacy was demonstrated in Siberian polecats (Wimsatt 2003) but more research is needed to evaluate its efficacy and safety in other species.

VI. Vaccination of Non-Domestic Carnivores : a Review

References Ahmed, R., Gray, D. 1996. Immunologic memory and protective immunity: understanding their relation. Science 272(5258):54-60.

Aiello, S.E. (ed) 1998. Vaccination of exotic mammals. In: Merck’s Veterinary Manual 8 th edition: 1427-1431.

Alexander, K.A., Kat, P.W., Frank, L.G., House, C., Appel, M.J.G. 1995. Evidence of canine distemper virus infection among free-ranging spotted hyaenas ( Crocuta crocuta ) in the Masai Mara, Kenya . Journal of Zoo and Wildlife Medicine 26(2):201-206.

American Veterinary Medical Association, 1966. Conclusions and recommendations of the panel of the symposium on canine distemper immunisation. Journal of the American Veterinary Medical Association 149(5):714-8.

Anand, R., Malik, P.K., Prasad, G., Mukherjee, S.K. 2000. Serosurvey for viral infections in endangered captive Asiatic lions and sympatric nondomestic carnivores from Western India. Proceedings of the American Association of Zoo Veterinarians: 443.

Anonymous. Preventive medicine programme Sacramento Zoo 1990.

Anonymous. 1978. Vaccine induced rabies in a raccoon. CDC Rabies Surveillance, Annual Summary 1978; 4.

Appel, M.J.G. 1969. Pathogenesis of canine distemper. American Journal of Veterinary Research 30(7):1167-1182.

Appel, M.J.G. 1978. CAV-2: a replacement for canine hepatitis vaccine. Norden News 53:4- 6.

Appel, M.J.G., Shek, W.R., Shesberadaran, H., Norrby, E. 1984. Measles virus and inactivated canine distemper virus induce incomplete immunity to canine distemper. Archives of Virology 82(1-2):73-82.

Appel, M.J.G. 1987. Virus Infections of Carnivores, Amsterdam; Elsevier Science Publications BV.

Appel, M.J.G., Scott, F.W., Carmichael, L.E. 1979. Isolation and immunization studies of a canine parvo-like virus from dogs with haemorrhagic enteritis. Veterinary Record 105(8):156- 159.

Appel, M.J.G., Yates, R.A., Foley, G.L., Bernstein, J.J., Santinelli, S., Spelman, L.H., Miller, L.D., Arp, L.H.

Anderson, M., Pearce-Kelling, S., Summers, B.A. 1994. Canine distemper epizootic in lions, tigers, and leopards in North America. Journal of Veterinary Diagnostic Investigations 6(3):277-288.

Appel, M.J.G., Montali, R.J. 1994. canine distemper and emerging morbillivirus diseases in exotic species. Proceedings of the American Association of Zoo Veterinarians Annual Conference :336-339.

VI. Vaccination of Non-Domestic Carnivores : a Review

Appel, M.J.G., Schultz, R.D., 1999. Forty years of canine vaccination. Advances in Veterinary Medicine 41: 309-324.

Armstrong, W.H., Anthony, C.H. 1942. An epizootic of canine distemper in a zoological park. Cornell Veterinarian 32:286.

Baer, G.M., Abelseth, M.K. and Debbie, J.G. 1971. Oral vaccination of foxes against rabies. American Journal of Epidemiology 93:487-490.

Baker GA et al. 1952. Immune response of ferrets to vaccination with egg-adapted distemper virus: I. Time of development of resistance to virulent distemper virus. Veterinary Medicine 47:463.

Barker, I.K., Povey, R.C., Voigt, D.R. 1983. Response of mink, skunk, red fox and raccoon to innoculation with mink virus enteritis, feline panleukopenia and canine parvovirus and prevalence of antibody to parvorvirus in wild carnivores in Ontario. Canadian Journal of Comparative Medicine 47(2):188-197.

Barker, I.K., and Parrish, C.R. 2001. Parvovirus infections. In: Williams, E.S. and Barker, I.K. (eds): Infectious diseases of wild mammals 3rd edition. Iowa State University Press:131- 146.

Barrett, T. 1999. Morbillivirus infections, with special emphasis on morbilliviruses of carnivores. Veterinary Microbiology 69(1-2):3-13.

Bassiri, M. Ahmad, S., Giavedoni, L., Jones, L., Saliki, J.T., Mebus, C., Yilma, T. 1993. Immunological responses of mice and cattle to Baculovirus-expressed F and H proteins of Rinderpest virus: lack of protection in the presence of neutralizing antibody. Journal of Virology 67(3):1255-1261.

Behlert, O., Behlert, C. 1981. Antikörperbesimmungen in einem Felidbestand nach vakzination mit zwei verschiedenen Panleukopenie-Impfstoffen. Verh ber Erkr Zootiere , 23:47-51.

Bildt, van de M.W.G., Kuiken, T., Visee, A.M., Lema, S., Fitzjohn, T.R, Osterhaus, A.D.M.E. 2002. Distemper and its effect on African wild dog conservation. Emerging infectious diseases 8(2):211-213.

Bengis, R.G., Kock, R.A., Fischer, J. 2002. Infectious animal diseases: the wildlife/livestock interface. Revue Scientifique et Technique Office International des Epizooties 21(1):53-65.

Bingham, J., Schumacher, C.L., Hill, F.W., Aubert, A. 1999. Efficacy of SAG-2 oral rabies vaccine in two species of jackal ( Canis adustus and Canis mesomelas ) Vaccine 17(6):551- 558.

Bittle, J.M. 1993: use of vaccines in exotic animals. Journal of Zoo and Wildlife Medicine 24(3):352-356.

Black, D.N., Pastoret, P.P., Gielkens, A.L.J., Skinner, M.A., Gaskell, R.M. 1993. Assesment of environmental impact from the use of live recombinant virus vaccines. EC-sponsored research on safety of genetically modified organisms: http://europa.eu.int/comm/research/quality-of-life/gmo/08-vaccines/08-07-project.html

Blasco, E., Lambot, M., Barrat, J., Cliquet, F., Brochier, B., Renders, C., Krafft, N., Bailly, J., Munier, M., Pastoret, P.P., Aubert, M.F. 2001. Kinetics of humoral immune response after

VI. Vaccination of Non-Domestic Carnivores : a Review rabies VR-G oral vaccination of captive fox cubs ( Vulpes vulpes ) with or without maternally derived antibodies against the vaccine. Vaccine 19(32):4805-15.

Bögel, K., Andral, L., Beran, G., Schneider, L.G., Wandeeler, A. 1982. Dog rabies elimination: a trend analysis and programme proposal prepared by a WHO working group. International Journal of Zoonoses 9(2):97-112.

Borst, G.H.A., Osterhaus, A.D.M.E., Walvoort, H.C., Reijnders, P.J.H., Van der Kamp, J.S. 1986. An outbreak of herpesvirus infection in harbour seals ( Phoca vitulina ). Journal of Wildlife Diseases 22(1):1-6.

Briggs, M.B., Ott, R.L. 1986. Feline leukemia infection in a captive cheetah and the clinical and antibody response of six captive cheetahs to vaccination with a subunit feline leukemia virus vaccine. Journal of the American Veterinary Medical Association 189(9):1197-9.

Briggs, M.B., 1986. Possible feline leukemia virus infection in a captive cheetah and the response of captive cheetahs to feline leukemia vaccination. Proceedings of the American Association of Zoo Veterinarians .

Budd, J. 1981. Distemper. In: Davis, Karstad and Trainer (eds), Infectious diseases of wild mammals 2nd edition. The Iowa State University press, Ames, IA:31-44.

Bunn, T.O., Ridpath, H.D., Beard, P.D. 1984. The relationship between rabies antibody titres in dogs and cats and protection from challenge. Rabies Information Exchange 11: 9-13.

Burroughs, R.E.J. 1992. Care of carnivores in captivity. In: McKenzie, A.A (ed): The capture and care manual. Wildlife decision support services, South Africa.

Bush, M., Montali, R.J., Brownstein, O., James, A.E., Appel, M.J.G. 1976; Vaccine-induced canine distemper in a lesser panda. Journal of the American Veterinary Medical Association 169(9):959-960.

Bush, M., Povey, R.C., Koonse, H. 1981. Antibody response to an inactivated vaccine for rhino- tracheitis, caliciviral disease, and panleukopenia in non-domestic felids . Journal of the American veterinary Medical Association 179(11):1203-05.

Bush, M., Montali, R.J., Reid, F.L., sumner, J.W., Yager, P.A., Phillips, L.G. 1985. Antibody response in zoo animals to a killed rabies vaccine. Proceedings of the American Association of Zoo Veterinarians Annual Conference:30.

Cameron, K.N., Campbell, M.K., Long, P.H., Munson, L., Chambers, A. Kroll, J.L., Summers, B.A. 1998. Canine distemper in a captive Indochinese tiger ( Panthera tigris corbetti ). Proceedings of the American Association of Zoo Veterinarians :201-202.

Carmichael, L.E., Joubert, J.C., Pollock, R.V.H. 1983. A modified live canine parvovirus vaccine. II. Immune response. Cornell Veterinarian 73: 13-29.

Carmichael, L.E., Schlafer, D.H., Hashimoto, A. 1994. Minute virus of canines (MVC, canine parvovirus type-1): pathogenicity for pups and seroprevalence estimate. Journal of Veterinary Diagnostic Investigation . 6(2):165-74.

Carmichael, L.E. 1999. Canine vaccines at a turning point-a personal perspective. Advances in Veterinary Medicine 41:289-307.

VI. Vaccination of Non-Domestic Carnivores : a Review

Carpenter, J.W., Appel, M.J.G., Erickson, R.C., Novilla, M.N. 1976; Fatal vaccine-induced distemper virus infection in black-footed ferrets. Journal of the American Veterinary Medical Association 169(9):961-964.

Castro, A.E. 2001. Other Herpesviruses. In: Williams E.S., Barker, I.K. (eds): Infectious Diseases of Wildlife 3rd edition. Iowa State University Press:175-178.

Chaffee, P.S. 1972. An outbreak of fox encephalitis in vaccinated wild canidae. Journal of Zoo Animal Medicine 3:5.

Chalmers, W.S.K., Baxendale, W. 1994. A comparison of canine distemper vaccine and measles vaccine for the prevention of canine distemper in young puppies. Veterinary Record 135:349-353.

Cherpillod, P. Tipold, A., griot-Wenk, M., Cardozo, C., Schmid, I, fatzer, R,. Schobesberger, M., Zurbriggen, R., Bruckner, L., Roch, F., VandeVelde, M., Wittek, R., Zurbriggen, A. 2000. DNA vaccine encoding nucleocapsid and surface proteins of wild type canine distemper virus protects its natural host against distemper. Vaccine 8(26):29927-2936.

Christensen, N.O. 1964. Some observations on diseases in carnivores in the Copenhagen zoo. Proceedings 5 th International Symposium on Diseases in Zoo-Animals 1963. Tijdschrift voor Diergeneeskunde 89 suppl. I.

Citino, S.B. 1986. Transient FeLV viremia in a clouded leopard. Journal of Zoo Animal Medicine 17:5-7.

Citino, S.B. 1988. Use of a subunit feline leukemia virus vaccine in exotic cats. Journal of the American Veterinary Medical Association 192(7):957.

Cole, R. 1998. Rethinking canine vaccinations. Veterinary Forum jan:52-57.

Collins, J.E., Leslie, P., Johnson, D., Nelson, D., Peden, W., Boswell, R., Draayer, H. 1984. Epizootic of adenovirus infection in American black bears. Journal of the American Veterinary Medical Association 185(11):1430-1432.

Cooper PE et al 1991. Comparaison de léfficacite des differents vaccins du chien, utilises sous forme monovalente ou associee, par evaluation des responses serologiques et apres epreuves virulentes 12, 22 et 26 mois apres vaccination. Bulletin Mensuel de la Societe Veterinaire Pratique de France 75:131-152.

Crawshaw, G.J., Mehren, K.G., Pare, J.A. 1996. Possible vaccine induced viral disease in cheetahs. Proceedings of the American Association of Zoo Veterinarians Annual conference:557-560 .

Cubas, Z.S. 1996. Special challenges of maintaining wild animals in captivity in South America 1996. Review of Science and Technology 15(1):267-87.

Curlee, J.F. 1999. Cross-species vaccination in wild and exotic animals. Advances in veterinary Medicine 41:551- 556.

Davis, J.W., Karstad, L.H., Trainer, D.O. 1981. Infectious Diseases of Wild Mammals 2 nd edition. Iowa State University Press.

Dawson, S., Willoughby, K., Gaskell, R.M., Wood, G., Chalmers, W.S. 2001. A field trial to assess the effect of vaccination against feline herpesvirus, feline calicivirus and feline

VI. Vaccination of Non-Domestic Carnivores : a Review panleukopenia virus in 6 week old kittens. J ournal of Feline Medicine and Surgery 3(1):17- 22.

Debbie, J.G. 1979. Vaccine induced rabies in a pet skunk. Journal of the American Veterinary Medical Association 175(4):376-7).

Department for Environment, Food and Rural affairs (DEFRA) 2001. Guidelines for vaccinating endangered species and promoting biosecurity in zoos (4 may 2001). www.defra.gov.uk

DEFRA, IZVG, RSPCA 2002. The options for a vaccination programme of seals against phocine distemper virus in response to predicted PDV outbreak in UK in 2002. www.defra.gov.uk

Dhein, C.R., Gorham, J.R. 1986. Host response to vaccination. Veterinary Clinics of North America. Small Animal Practice 16: 1227-1245.

Dodds, W.J. 1999. More bumps on the vaccine road. Advances in Veterinary Medicine 41:715-32.

Dolensek, E. 1978 History of medicine in the New York zoological park. The Journal of Zoo Animal Medicine 9(1):18-19.

Dorny, P., Fransen, J., 1989. Toxoplasmosis in a Siberian tiger ( Panthera tigris altaica ). Veterinary Record 125(26-27):647.

Dubey, J.P., gendron-Fitzpatrick, A.P., Lenhard, A.L., Bowman, D. 1988. Fatal toxoplasmosis and enteroepithelial stages of Toxoplasma gondii in a Pallas cat ( Felis manul ). Journal of Protozoology 35(4):528-530.

Dunbar, M.R., Cunningham, M.W., Roof, J.C. 1998. Seroprevalence of selected disease agents from free-ranging black bears in Florida. Journal of Wildlife Diseases 34(3):612-9.

Dunn, J.L. 1990. Bacterial and mycotic diseases of cetaceans and pinnipeds. In: Dierauf LA (ed): CRC Handbook Of Marine Mammal Medicine: Health, Disease, and rehabilitation. Boca Raton, CRC Press:73-88.

Durchfeld, B. Baumgartner, W., Herbst, W., Brahm, R. 1990. Vaccine associated canine distemper infection in a litter of African hunting dogs ( Lycaon pictus ) Zentralblatt für Veterinärmedizin Reich B 37:203-212.

Ek-Kommonen, C., Rudback, E., Antilla, M., Aho, M., huovilainen, A., Canine distemper of vaccine origin in European mink, Mustela lutreola - a case report. Veterinary Microbiology apr 2;92(3):289-93.

Elston, T., Rodam, H., Flemming, D., Ford, R.B., Hustead, D.R., Richards, J.R., Rosen, D.K., Scherk-Nixon, M.A., Scott, P.W. 1998. 1998 Report of the American association of feline practitioners and academy of feline medicine advisory panel on feline vaccines. Journal of the American Veterinary Medical Association 212(2):227- 41.

Erlewein, D.L. 1981. Post vaccinal rabies in a cat. Feline Practitioner 11(2):16-21.

Federoff, N.E. 2001. Antibody response to rabies vaccination in captive and free-ranging wolves ( Canis lupus ). Journal of Zoo and Wildlife Medicine 32(1):127-129, 2001.

VI. Vaccination of Non-Domestic Carnivores : a Review

Fischer, L., Tronel, J.P., Pardo-David, C., Tanner, P., Colombet, G., Minke, J., Audonnet, J.C. 2002. Vaccination of puppies born to immune dams with a canine adenovirus-based vaccine protects against a canine distemper virus challenge. Vaccine 20(29-30):3485-97.

Fischer, L., Tronel, J.P., Minke, J., Barzu, S., Baudu, P., Audonnet, J.C. 2003. Vaccination of puppies with a lipid-formulated plasmid vaccine protects against a severe canine distemper virus challenge. Vaccine 7;21(11-12):1099-102.

Fix, A.S., Riordan, D.P., Hill, H.T., Gill, M.A., Evans, M.B. 1989. Feline panleukopenia virus and subsequent CDV infection in two snow leopards . Journal of Zoo and Wildlife Medicine 20(3):273-281.

Fletcher, K.C., Eugster, A.K., Schmidt, R.E., Hubbard, G.B. 1979. Parvovirus infection in maned wolves. Journal of the American Veterinary Medical Association 175(9):897-900.

Follmann, E.H., Ritter, D.G., Baer, G.M. 1988. Immunization of arctic foxes ( Alopex lagopus ) with oral rabies vaccine. Journal of Wildlife Diseases 24(3):477-83.

Fowler, M. 1974. Preventive vaccination program for captive wild felids. The World’s cats vol 3 nr 3 (1977) Proc. 3 rd International Symposium on the World’s Cats april 1974.

Fowler, M.E. 1986. Carnivora. In: Fowler ME (ed): Zoo and Wild Animal Medicine Current therapy 2. Saunders comp. 203-204.

Fowler, M.E. 1989. Llama basics. In: Kirk RW (ed): Current Veterinary Therapy X – Small Animal Practice . Philadelphia; Saunders Co:734-737.

Fowler, M.E. (ed) 1993. Zoo and Wild Animal Medicine Current therapy 3, Saunders Co.

Franke, V. 1989. Profylaxe der Staupe bei zootieren. Berl. Munch. Tieratztl. Wschr 102, 056- 058.

Frankenhuis, Visee, A.M. 1985. Entingen Bij Exotische Dieren. Diergeneeskundig Memorandum 32:(1):138.

Fraser, C.M. (ed). 1991. Vaccination of exotic mammals. Merck veterinary manual seventh edition:1015-1019.

Gabrisch, K. Zwart, P. 1987. Krankheiten der Wildtiere . Schlutersche GmbH & Co. KG, Hannover.

Geyer, Matern 2001. pers. comm. In: Arbeitstagung der zootierartze im deutschsprachigen raum , 2-4 november 2001, tagungsbericht:166.

Gillespie, J.H. Baker, J.A., Burgher, J.A., Robson, D., Gilman, B. 1958. The immune response of dogs to distemper virus. Cornell Veterinarian 48:103-126.

Gillespie, J.H. 1966.The significance of passive immunity and the biological tests used in the study of distemper. Journal of the American Veterinary Medical Association 149(5):623-628.

Goodrich, J.M., Williams, E.S., Buskirk, S.W. 1994. Effects of a modified live virus canine distemper vaccine on captive badgers. Journal of Wildlife Diseases 30(4):492-496.

Goltenboth, R. 1992. Preventive vaccination problems in zoo animals. Erkr der zootiere 93- 96.

VI. Vaccination of Non-Domestic Carnivores : a Review

Goltenboth, R. 1981. Veterinary prophylaxis in Zoological Garden of Berlin. Erkr. der Zootiere 17-21.

Gorham, J.R., 1966. Duration of vaccination immunity and the influence on subsequent prophylaxis. Journal of the American Veterinary Medical Association 149(5):699-704.

Goss, L.J., 1942. Diagnosis and treatment of diseases of wild animals in captivity. Cornell Veterinarian 32:155-161.

Gray, C. 1972. Immunization of exotic felidae for panleukopenia. Journal of Zoo Medicine 3:14-15.

Green, J.S., Bruss, M.L., Evermann, J.F., Bergstrom, P.K. 1984. Serologic response of captive coyotes ( Canis latrans say ) to canine parvovirus and accompanying profiles of canine coronavirus titres. Journal of Wildlife Diseases 20(1):6-11.

Greenacre, C.B. 2003. Incidence of adverse events in ferrets vaccinated with distemper or rabies vaccine:143 cases (1995-20010). Journal of the American Veterinary Medical Association 223(5):663-665.

Greene, C.E. 1990. Immunoprophylaxis and immunotherapy. In: greene, C.E. (ed): Infectious diseases of the dog and cat . Philadelphia; W.B. Saunders:291-299.

Gulland, F.M., Lowenstine, L.J., Lapointe, J.M., Spraker, T., King, D.P. 1997. Herpesvirus infection in stranded Pacific harbour sels of Coastal california . Journal of Wildlife Diseases 33:450-458.

Gumley, N. 1999. Update on vaccination protocols. Canadian Veterinary Journal 40:323-324.

Haas, L., Hofer, H., East, M., Wohlsein, P., Liess, B., Barrett, T. 1996. Canine distemper infection in Serengeti spotted hyaenas. Veterinary Microbiology 49(1-2):147-152.

Halbrooks, R.D., Swango, L.J., Schnurrenberger, P.R., Mitchell, F.E., Hill, E.P. 1981. Response of gray foxes to modified live-virus canine distemper vaccines. Journal of the American Veterinary Medical Association 179(11):1170-1174.

Harder, T.C., Vos, H.W., de Swart, R.L., Osterhaus, A.D.M.E. 1997. Age related disease in recurrent outbreak of phocid herpesvirus type-1 infections in a seal rehabilitation centre: evaluation of diagnostic methods. Veterinary Record 140:500-503.

Harrenstien, L. Munson, L., Lucash, C.F., Ramsay, E.C., Kania, S.A., Potgieter, L.N.D. 1995 Antibody responses of red wolves to canine distemper virus and canine parvovirus vaccination. Proceedings of the American Association of Zoo Veterinarians Annual Conference :427-8.

Harrenstien, L.A., Munson, L., Lucash, C.F., Kania, S.A., Potgieter, L.N. 1997. Antibody responses of red wolves to canine distemper virus and canine parvovirus vaccination. Journal of Wildlife Diseases 33(3):600-605.

Harrison, T.M., Mazet, J.A., Holekamp, K.E., Dubovi, E., Engh, A.L., Nelson, K., Horn van, R.C., Munson, L. 2002. Expossure of spotted hyaenas ( Crocuta crocuta ) to feline and canine viruses in the Masai Mara National reserve, Kenya. Proceedings of the American Association of Zoo Veterinarians Annual Conference :10-11.

VI. Vaccination of Non-Domestic Carnivores : a Review

Harthorn, S., Wimsatt, J., Biggins, D.E., Godbey, J.L., Branvold, H. 1999. Evaluation of modifie live canine distemper vaccine boostering and chal lenge in black-footed ferrets (Mustela nigripes ) previously vaccinated with a killed vaccine Proceedings of the American Association of Zoo Veterinarians Annual Conference:356-357 .

Heerden, van, J., Swart, W.H., Meltzer, D.G.A. 1980. Serum antibody levels before and after administration of live canine distemper vaccine to the wild dog Lycaon pictus. Journal of the South African Veterinary Medical Association 51(4):283-284.

Heerden van J., Swart, W.H., Meltzer, D.G. 1988. Serum antibody levels before and after administration of live canine distemper vaccine to the wild dog Lycaon pictus . Journal of the South African Veterinary Association 193(3):332-3.

Heerden van, J., Bingham, J., Vuuren van, M., Burroughs, R.E., Stylianides, E. 2002. Clinical and serological response of wild dogs ( Lycaon pictus ) to vaccination against canine distemper, canine parvovirus infection and rabies. Journal of the South African Veterinary Association 73(1):8-12.

Henke, S.E. 1997. Effects of modified live virus canine distemper vaccine in gray foxes . Journal of Wildlife Rehabilitation 20:3-7.

Hindle, E., Findlay, G.M. 1932. Studies on feline distemper. Journal of comparative pathology and therapy 45:11- 26.

Hoover, J.P., Castro, A.E., Nieves, M.A. 1985. Serologic evaluation of vaccinated American river otters. Journal of the American Veterinary Medical Association 187(11): 1162-1165.

Hustead, D.R., Carpenter, T., Sawyer, D.C., Bain, F.T., Henry, S.T., Huxsol, D.L., Klingborg, D.J., McKissick, G.E., McNutt, R.L., Niles, D.E., Short, C.R. 1999. Vaccination issues of concern to practitioners. Journal of the American Veterinary Medical Association 214(7):1000-1002.

Itakura, C., Nakamura, K., Nakatsuka, J., Goto, M. 1979. Distemper infection in lesser pandas due to the administration of canine distemper live vaccine. Journal of the Nippon Medical school 41(5): 561-566.

Janssen, D.L., Bartz, C.R., Bush, M., Marchwicki, R.H., Grate, S.J., Montali, R.J. 1982. Parvovirus enteritis in vaccinated juvenile bush dogs. Journal of the American Veterinary Medical Association 181(11):1225-7.

Johnson, R.P., Povey, R.C., 1985. Vaccination against feline rhinotracheitis in kittens with maternally derived feline viral rhinotracheitis antibodies. Journal of the American Veterinary Medical Association 186(2):149-152.

Jones, L., Giavedoni, L., Saliki, J.T., Brown, C., Mebus, C., Yilma, T. 1993. Protection of goats against peste des petites ruminants with a vaccinia virus double recombinant expressing the F and H genes of rinderpest virus. Vaccine 11(9):961-4.

Jones, L., Tenorio, E., Gorham, J., Yilma, T. 1997. Protective vaccination of ferrets against canine distemper with recombinant pox virus vaccines expressing the H or F genes of rinderpest virus. American Journal of Veterinary Research 58(6):590-593.

Joslin, J., Amand, W., Bush, M., Haigh, J., Miller, E., Stoskopf, M. 1990. Veterinary Standards Committee of the American Association of Zoo Veterinarians: Guidelines for zoo

VI. Vaccination of Non-Domestic Carnivores : a Review and aquarium veterinary medical programs and veterinary hospitals. Supplement to J of Zoo and Wildl med 21(3).

Junge, R.E. 1995. Preventive Medicine Recommendations American Association of Zoo Veterinarians Infectious Diseases Committee.

Kadoi, K., Kiryu, M., Inaba, Y. 1998. Antibody response of lions inoculated with inactivated calicivirus vaccine experimentally prepared. New Microbiology 21(2):147-51.

Karesh, W.B., Bottomley, G. 1983. Vaccine induced anaphylaxis in a Brazilian Jaguar. Journal of Zoo Animal Medicine 14(4):133-137.

Kazacos, K.R., Thacker, H.L., Shivaprasad, H.L., Burger, P.P. 1981. Vaccination induced distemper in Kinkajous. Journal of the American Veterinary Medical Association 179(11): 1166-9.

Kennedy, S., Smyth, J.A., McCullough, S.J., Allan, G.M., McNeilly, F., McQuaid, S. 1988. Confirmation of cause of recent seal deaths. Nature 335(6189) :404.

Kennedy, S. 2001. Morbillivirus infections in aquatic mammals. In: Williams, E.S. & Barker, I.K. (eds): Infectious diseases of wild mammals 3 rd edition. Iowa State University Press.

Kennedy-Stosskopf, S. 1996: Emerging viral infections in large cats. In: Fowler, M.E.: Zoo and Wild Animal Medicine, Current therapy 4, Saunders Comp:401-404.

Kinsel, M.J., Boehm, J.R., Harris, B., Murnane, R.D. 1997. Fatal Erysipelothrix rhusiopathiae septicemia in a captive Pacific white-sided dolphin (Lagenorhyncus obliquidens). Journal of Zoo and Wildlife Medicine 28(4):494-7.

Klös, H.G., Lang, E.M. 1981. Handbook of Zoo Medicine: Disease and Treatment of Wild Animals in Zoos, Game Parks, Circuses and Private Collections . Van Nostrand Reinhold International.

Knobel, D.L., du Toit, J.T., Bingham, J. 2002. Development of a bait and baiting system for delivery of oral rabies vaccine to free-ranging African wild dogs ( Lycaon pictus ). Journal of Wildlife Diseases 38(2):352-62.

Kommonen, C.E., Sihvonen, L., Pekkanen, K., Rikula, U., Nuotio, L. 1997. Outbreak of canine distemper in vaccinated dogs in Finland. Veterinary Record 141(15):380-383.

Krakowka, S., R. Olsen, A. Confer, A. Koestner, and B. McCullough. 1975. Serologic response to canine distemper viral antigens in gnotobiotic dogs infected with canine distemper virus. Journal of Infectious Diseases 132:384-392.

Krakowka, S., Olsen, R.G., Axthelm, M.K., Rice, J., Winters, K. 1982. Canine Parvovirus infection potentiates distemper encephalitis attributable to MLV vaccine. Journal of the American Veterinary Medical Association 180(2):137-140.

Krakowka, S., Long, D., Koestner, A. 1978. Influence of transplacentally acquired antibody on neonatal susceptibility to canine distemper virus in gnotobiotic dogs. Journal of Infectious Diseases 137(5):605-8.

Kruth, S.A., Ellis, J.A. 1998. Vaccination of dogs and cats: General Principles and duration of immunity. Canadian Veterinary Journal 39(7):423-6.

VI. Vaccination of Non-Domestic Carnivores : a Review

Lambot, M., Blasco, E., Barrat, J., Cliquet, F., Brochier, B., Renders, C., Krafft, N., Bailly, J., Munier, M., Aubert, M.F., Pastoret, P.P. 2001. Humoral and cell-mediated responses of foxes (Vulpes vulpes ) after experimental primary and secondary oral vaccination using SAG2 and V-RG vaccines. Vaccine 19(13-14):1827-1835.

Lilenbaum, W., Monteiro, R.V., Ristow, P., Fraguas, S., Cardoso, V.S., Fedullo, L.P. 2002. Leptospirosis antibodies in mammals from Rio de Janeiro Zoo, Brazil. Research in Veterinary Science 73(3):319-21.

Linhart SB, Wlodkowski JC, Kavanaugh DM, Motes-Kreimeyer L, Montoney AJ, Chipman RB, Slate D, Bigler LL, Fearneyhough MG. 2002. A new flavor-coated sachet bait for delivering oral rabies vaccine to raccoons and coyotes. Journal of Wildlife Diseases 38(2):363-77.

Luff, P.R., Wood, G.W., Thornton, P.H., 1987. Canine parvovirus serology: collaborative assay. Veterinary Record 120(12):270-273.

Lynch, M.J., Obendorf, D.L., Statham, P., Reddacliff, G.L. 1993. An evaluation of a live Toxoplasma gondii vaccine in Tammar wallabies ( macropus eugenii ). Australian veterinary journal 70(9):352-353.

Lynch, M.J. Obendorf, D.L., Statham, P., Reddacliff, G.L. 1993; Serological responses of Tammar wallabies ( macropus eugenii ) to inoculation with an attenuated strain of Toxoplasma gondii . Proceedings of the American Association of Zoo Veterinarians Annual Conference:185-8.

Maack, D., Böer, M., Brandt, H.P., Liess, B. 2000. Morbillivirus infections in German zoos: prevalence in carnivores and vaccination trials in pantherid cats. Proceedings of the European Association of Zoo Veterinarians Annual Conference .

Machida, N., Izumisawa, N., Nakamura, T., Kiryu, K. 1992. Canine distemper virus infection in a masked palm civet ( Paguma larvata ). Journal of Comparative Pathology 107(4):439-443.

Maia, O.B., Gouveia, A.M.G. 2001. Serologic response of maned wolves ( Chrysocyon brachyurus ) to canine distemper virus and canine parvovirus vaccination. Journal of Zoo and Wildlife Medicine 32(1): 78-80.

Marsilio, F., Tiscar, P.G., Gentile, L., Roth, H.U., Boscagli, G., Tempesta, M., Gatti, A. 1997. Serologic survey for selected viral pathogens in brown bears from Italy. Journal of Wildlife Diseases 33(2):304-7.

Martin, M.L. 1985. Canine coronavirus enteritis and a recent outbreak following modified live virus vaccination. Compendium on Continuing Education for the Practicing Veterinarian 7:1012-1017.

Martina, B.E., Airikkala, M.I., Harder, T.C., Amerongen van, G., Osterhaus, A.D.M.E. 2001. A candidate phocid herpesvirus vaccine that provides protection against feline herpesvirus infection. Vaccine 20(5-6):943-8.

Martina BE, van de Bildt MW, Kuiken T, van Amerongen G, Osterhaus AD. Immunogenicity and efficacy of Recombinant subunit vaccines against phocid herpesvirus type 1. Vaccine . 2;21(19-20):2433-2440.

VI. Vaccination of Non-Domestic Carnivores : a Review

Mc Caw, D.L., Thompson, M., Tate, D., Bonderer, A., Chen, Y. 1998. Serum distemper virus and parvovirus antibody titres among dogs brought to a veterinary hospital for revaccination. Journal of the American Veterinary Medical Association 213(1):72-75.

Mc Cormick, A.E. 1983. Canine distemper in African Cape hunting dogs ( Lycaon pictus )- Possibly vaccine induced. Journal of Zoo Animal Medicine 14(2):66-71.

Mc Innes, E.F., Burroughs, R.E., Duncan, N.M. 1992. Possible vaccine-induced canine distemper in a South American bush dog. Journal of Wildlife Diseases 28(4):614-617.

Mehren K, 1984. Personal communication in: Appel MJG (ed) Virus infections of carnivores . Meehan, T.P., Hungerford, L.L., Smith, C.L. 1998. Risk factors for canine distemper virus seropositivity in zoo cats. Proceedings of the American Association of Zoo Veterinarians Annual Conference :133-134.

Meltzer, D.G.A. 1996. Medical management of a cheetah breeding facility in South Africa. In: Fowler M (ed): Zoo and wild animal medicine – Current therapy 4:415-423.

Meunier, P.C., Cooper, B.J., Appel, M.J., Lanieu, M.E., Slauson, D.O. 1985. Pathogenesis of canine parvovirus enteritis. II. Sequential virus distribution and passive immunization studies. Veterinary Pathology 22(6):617-624.

Miller, R.E. 1989. Immunisation of wild animal species against common diseases. In: Kirk RW (ed): Current Veterinary Therapy X – Small Animal Practice:1361-1362.

Miller, R.E., Anderson, N.L. 2000. Immunization of wild mammal species against common diseases. In: Kirk RW (ed): Current Veterinary Therapy XIII – Small Animal Practice :1123.

Mishima, M., Xuan, X., Yokoyama, N., Igarashi, I., Fujisaki, K., Nagasawa, H., Mikami, T. 2002. Recombinant feline herpesvirus type 1 expressing Toxoplasma gondii ROP2 antigen inducible protective immunity in cats. P arasitological research 88(2):144-9.

Montali, R.J., Bartz, C.R., Teare, J.A., Allen, J.T., Appel, M.J., Bush, M. 1983. Clinical trials with canine distemper vaccines in exotic carnivores. Journal of the American Veterinary Medical Association 183(11):163-166.

Montali, R.J., Bartz, C.R., Bush, M. 1987. Canine distemper virus. In: Virus infections of carnivores . Elsevier, Amsterdam:437-443.

Montali, R.J., Tell, L., Bush, M., Cambre, R.C., Kenny, D., Sutherland-Smith, M., Appel, M.J.G. 1994. Vaccination against canine distemper in exotic carnivores: successes and failures. Proceedings of the American Association of Zoo Veterinarians Annual Conference :340-344.

Montali, R.J., Heuschele, W., Williams, E., Lance, W. 1998. Development, production and safety evaluation of canine distemper vaccines for use in exotic carnivores final report, September 1998, American Association of Zoo Veterinarians Canine Distemper Virus Subcommittee, Media, Pennsylvania.

Moss, B. 1996. Genetically engineered poxviruses for recombinant gene expression, vaccination and safety. Proceedings of the National Academy of Sciences USA 93:11341- 11348.

VI. Vaccination of Non-Domestic Carnivores : a Review

Munson, L., Appel, M.J.G., Carpenter, M.A, Roelke-Parker, M. 1995. Canine Distemper in wild felids. Proceedings of the American Association of Zoo Veterinarians Annual Conference :135-136.

Murphy, F.A., Gibbs, E.P., Horzinek, M.C., Studdert, M.J. (eds) 1999. Vaccination against viral diseases. In: Veterinary Virology 3 rd edition. New York, Academic Press.

North, D.C. 1978. Cat flu vaccine hazard (correspondence). Veterinary Record 102(6):134. Ocholi, R.A., Kalejaiye, J.O., Okewole, P.A. 1989. Acute disseminated toxoplasmosis in two captive lion ( Panthera leo ) in Nigeria. Veterinary Record 124(19):515-516.

Olson, P., Finnsdottir, H., Klingeborn, B., Hedhammar, A. 1997. Duration of antibodies elicited by canine distemper vaccination in dogs. Veterinary Record 141(25):654-655.

Olson, P., Klingeborn, B., Hedhammar, A. 1988. Serum antibody response to canine parvovirus, canine adenovirus-1 and canine distemper in dogs with known status of immunisation: study of dogs in Sweden. American Journal of Veterinary Research 49(9):1460-1466.

Osofsky, S.A., Hardy, W.D., Hirsh, K.J. 1994. Serologic evaluation of free-ranging lions (Panthera leo ), leopards ( panthera pardus ) and cheetahs ( Acinonyx jubatus ) for feline lentivirus and feline leukemia virus in Botswana. Proceedings of the American Association of Zoo Veterinarians Annual Conference :398-402.

Osterhaus, A.D.M.E., Yang, H., Spijkers, H.E., Groen, J., Teppema, J.S., van Steenis, G. 1985.The isolation and partial characterization of a highly pathogenic herpesvirus from the harbor seal (Phoca vitulina). Archives of Virology 86(3-4):239-51.

Osterhaus, A.D.M.E., Vedder, E.J. 1988. Identification of virus causing recent seal deaths. Nature 335(6185):20.

Osterhaus, A.D.M.E., Groen, J., Vries de, P., UytdeHaag, F.G., Klingeborn, B., Zarnke, R. 1988. Canine distemper virus in seals. Nature 335(6189):403-404.

Osterhaus, A.D.M.E., Visser, I.K., Swart de, R.L., Bressem van, M.F., Bildt van de, M.W., Orvell, C., Barrett, T., Raga, J.A. 1992. Morbillivirus threat to Mediterranean monk seals? Veterinary Record 30(7):141-142.

Osterhaus, A.D.M.E., Uyt de Haag, F.G.C.M., Visser, I.K.G., Vedder, E.J., Reijnders, P.J., Kuiper, J. et al. 1989. Seal vaccination success. Nature 337(6202): 21.

Paoletti, E. 1996. Applications of poxvectos to vaccination: an update. Proceedings of the National Academy of Sciences, USA 93:11349-11353.

Pardo, M.C., Bauman, J.E., Mackowiak, M. 1997. Protection of dogs against canine distemper by vaccination with a canarypox virus recombinant expressing canine distemper virus fusion and hemaglutinin glycoproteins. American Journal of Veterinary Research 58(8): 833-6.

Pare, J.A., Barker, I.K., Crawshaw, G.J., McEwen, S.A., Carman, P.S., Johnson, R.P. 1999. Humoral response and protection from experimental challenge following vaccination of raccoon pups with a modified-live canine distemper virus vaccine. Journal of Wildlife Diseases 35(3):430-439.

VI. Vaccination of Non-Domestic Carnivores : a Review

Parrish, C.R., Leathers, C.W., Pearson, R., Gorham, J.R. 1987. Comparison of feline panleukopenia virus, canine parvovirus, racoon parvovirus and mink enteritis and their pathogenicity for mink and ferrets. American Journal of Veterinary Research 48(10):1429-35 .

Pastoret, P.P., Brouchier, B., Aguilar-Setien, A., Blancou, J. 1997. Part 2. Vaccination against rabies. In: Pastoret, P.P., Blancou, J., Vannier, P., Verschueren, C. (eds): Veterinary Vaccinology , Elsevier, Amsterdam. chapter 18:616-628.

Pearson, G.L. 1977. Vaccine indused canine distemper virus in black-footed ferrets. Journal of the American Veterinary Medical Association 170(2):103,106,109.

Pedersen, N.C., Emmons, R.W., Selcer, R., Woodie, J.D., Holliday, T.A., Weiss, M. 1978. Rabies vaccine virus infection in three dogs. Journal of the American Veterinary Medical Association 172(9):1092-1096.

Pettan, K.C.B., Jessup, D.A., Lowenstine, L.J., Pedersen, N.C. 1992. Feline leukemia virus infection in a free ranging cougar. Proceedings of the American Association of Zoo Veterinarians : 136-138.

Pfizer 1998. Duration of Immunity in Companion Animals after natural infection and vaccination. www.pfizer.com .

Phillips, L.G. 1989. Preventive Medicine in non-domestic carnivores. In: Kirk RW (ed): Current Veterinary Therapy X– Small Animal Practice . Philidelphia; Saunders Co: 727-734.

Phillips, T.R., Jensen, J.L., Rubino, M.J., Yang, W.C., Schultz, R.D. 1989a. Effects of vaccines on the canine immune system. Canadian Journal of Veterinary Research 53(2):154-160.

Piercy, S.E. 1961. An appraisal of the value and method of use of living attenuated canine distemper vaccines. Veterinary Record 73:944-949.

Pollock, R.V.H. & Carmichael, L.E. 1990. Enteric viruses. In: Green CE (ed): Infectious diseases of the dog and cat . Saunders, Philadelphia: 226-283.

Pollock, R.V.H. & Carmichael, L.E. 1983. Use of modified live feline panleukopenia virus vaccine to immunize dogs against canine parvovirus. American Journal of Veterinary Research 44(2):169-175.

Pollock, R.V.H. & Carmichael, L.E. 1982. Maternally derived antibody to canine parvovirus: transfer, decline and interference with immunization. Journal of the American Veterinary Medical Association 180(1):37-43.

Porter, D.D., and Larsen, A.E. 1990. Mink parvovirus infections. In: Thijssen, P. (ed): CRC handbook of parvoviruses , vol 2, Boca Raton, Fl: 87-101.

Poston, R.P., England, J.J. 1992. Veterinary Diagnostic Virology , Mosbey Year Book, St Lewis: 135-138.

Povey, R.C., Davis, E.V. 1977. Panleukopenia and respiratory infections in wild felids. In: The World’s cats , Eton, R.L. (ed). The carnivore research institute, Burke museum of seattle, WA 3:120-128.

Prydie J. 1966 Persistence of antibodies following vaccination against canine distemper and the effect of re-vaccination. Veterinary Record 78(14):486-8.

VI. Vaccination of Non-Domestic Carnivores : a Review

Reddacliff, G.L., Parker, S.J., Dubey, J.P., Nicholls, P.J., Johnson, A.M., Cooper, D.W. 1993. An attempt to prevent acute toxoplasmosis in macropods by vaccination with Hammondia hammondi. Australian Veterinary Journal 70(1): 33-35.

Rikula, U., Nuotio, L., Sihvonen, L. 2000. Canine distemper virus neutralising antibodies in vaccinated dogs. Veterinary Record 147(2):598-603.

Rikula, U, Sihvonen, L., Voipio, H.M., Nevalainen, T. 1996. Serum antibody response to canine distemper virus vaccines in beagle dogs . Scandinavian Journal of Laboratory Animal science 23(1):31-33.

Roelke-Parker, M.E., Munson, L., Packer, C., Kock, R., Cleaveland, S., Carpenter, M., O’Brien, S.J., Pospischil, A., Hofmann-Lehmann, R., Lutz, H., et al. 1996. A canine distemper virus epidemic in Serengeti lions ( Panthera leo ). Nature 379(6564):441-445.

Rupprecht, C.E., Gilbert, J., Pitts, R., Marshall, K.R., Koprowski, H. 1990. Evaluation of an inactivated rabies vaccine in domestic ferrets. Journal of the American Veterinary Medical Association 196(10):1614-1616.

Rupprecht, C.E. 1996. International meeting on research advances and rabies control in the Americas. Emerging Infectious diseases 2(3):243.

Rupprecht, C.E., Stohr, K., Meredith, C. 2001. Rabies. In: Williams, E.S., Barker, I.K: Infectious diseases of wild mammals, 3 rd edition, Iowa State University Press: 3-36.

Schofield, F.W. 1949. Virus enteritis in mink. North American Veterinarian 30:651-654. Schroeder, H.D. 1974. Latest developments in immunoprophylaxis for zoo animals. Verhandlungsbericht XVI Internationalen Symposiums Ueber Erkrankungen Zootiere, Erfurt. Berlin: Akademie Verlag :155-165.

Schubert, C.A. 1995. Effect of CDV on an urban raccoon population. Proceedings of the American Association of Zoo Veterinarians Annual Conference:493 .

Schultz, R.D. 1998. Current and future canine and feline vaccination programs. Veterinary Medicine 93(3):233-254.

Scott, F.W. & Geissinger, C.M. 1999. Long-term immunity in cats vaccinated with an inactivated trivalent vaccine. American Journal of Veterinary Research 60(5):652-8.

Scott, W.A., Csiza, C.K., Gillespie, J.H. 1970. Maternally derived immunity to feline panleukopenia. Journal of the American Veterinary Medical Association 156(4): 439-453.

Scott, W.A. 1979. Use of vaccines in exotic species. Veterinary Record 104(9):199.

Sedgewick, C.J. 1966. An introduction to zoo practice. Modern veterinary Practice 37:39.

Sedgewick, C.J., Young, W.A. 1968. Distemper outbreak in a zoo. Modern Veterinary Practice 49:39.

Shotts, E.B. 1981. Leptospirosis. In: Davis JW, Karstad LH, Trainer DO (eds): Infectious diseases of wild mammals , second edition. Ames, IA; Iowa State University press:97-101.

VI. Vaccination of Non-Domestic Carnivores : a Review

Sikarski, J.G., Lowrie, C., Kennedy, F., Brady, G. 1991. Canine distemper in a vaccinated red panda ( Ailuris fulgens fulgens ). Proceedings of the Association of American Zoo veterinarians Annual Conference:292-3.

Silva, J.R., Ogassawara, S., Marvulo, M.F.V., Ferreira-Netto, J.S., Dubey, J.P. 2001. Toxoplasma gondii antibodies in exotic wild felids from Brazilian zoos. Journal of Zoo and Wildlife Medicine 32(3):349-351.

Smith, C.A. 1995. Are we vaccinating too much? Journal of the American Veterinary Medical Association 207(4):421-425.

Spencer, J.A., Burroughs, R. 1991. Antibody response of captive cheetahs to modified live feline virus vaccine. Journal of Wildlife Diseases 27(1):578-83.

Spencer, J.A., Burroughs, R. 1992. Antibody response to canine distemper vaccination in African wild dogs. Journal of Wildlife Diseases 28(3):443-4.

Spencer, J.A. 1991. Antibody response to modified-live canine adenovirus vaccine in African hunting dogs ( Lycaon pictus ). Zentralblatt fur Veterinarmedizin 38(6):477-9.

Spencer, J.A., Burroughs, R. 1992. Decline in maternal immunity and antibody response to vaccine in captive cheetah ( Acinonyx jubatus ) cubs. Journal of Wildlife Diseases 28(1):102- 104.

Steck, F., Wandeler, A., Bichsel, P., Capt, S., Schneider, L. 1982. Oral immunization of foxes against rabies. A field study. Zentralblatt Veterinaermedizin 29(5):372-396.

Steelman HG, Henke SE, Moore GM. 1998. Gray fox response to baits and attractants for oral rabies vaccination. Journal of Wildlife Diseases 34(4):764-70.

Steinel, A., Munson, L., van Vuuren, M., Truyen, U. 2000. Genetic characterization of feline parvovirus sequences from various carnivores. Journal of General Virology 81(Pt 2):345-50.

Steinel, A., Parrish, C.R., Bloom, M.E., Truyen, U. 2001. Parvovirus infections in wild carnivores. Journal of Wildlife Diseases 37(3):594-607.

Stephensen, C.B., Welter, J., Thaker, S.R., Taylor, J., Tartaglia, J., Paoletti, E. 1997. Canine distemper virus (CDV) infection of ferrets as a model for testing morbillivirus vaccine strategies: NYVAC- and ALVAC-based CDV recombinants protect against symptomatic infection. Journal of Virology 71(2);1506-1513.

Sutherland-Smith, M.R., Rideout, B.A., Mikolon, A.B., Appel, M.J.G., Morris, P.J., Shima, A.L., Janssen, D.J. 1997. Vaccine induced canine distemper in European mink ( Mustela lutreola ). Journal of Zoo and Wildlfe Medicine 28:312-319.

Sutter, G. Moss, B. 1992. Nonreplicating vaccinia vector efficiently expresses recombinant genes. Proceedings of the National Academy of Sciences, USA 89:10847-10851.

Swanson 1999. Toxoplasmosis and neonatal mortality in Pallas’ cats: a survey of North American zoological institutions. Proceedings of the American Association of Zoo Veterinarians .

Taylor, D.R., Martin, R.B. 1987. Effects of veterinary fences on wildlife conservation in Zimbabwe. Environmental management 11:327-334.

VI. Vaccination of Non-Domestic Carnivores : a Review

Tham, K.M., Studdert, M.J., 1987. Antibody and cell-mediated response to feline herpesvirus1 following inactivated vaccine and challenge. Journal of Veterinary Medicine . 34:585-597.

Thomas-Baker, B. 1985. Vaccination induced distemper in maned wolves, vaccination induced corneal opacity in a maned wolf. Proceedings of the American Association of Zoo Veterinarians Annual Conference :53.

Tiger information centre: www.5tigers.org/zoos/husbandry_manual/husman2a.htm

Tizard, I. 1990. Risks associated with use of live vaccines. Journal of the American Veterinary Medical Association 196(11):1851-1858.

Tizard, I., Ni, Y. 1998. The use of serologic testing to assess immune status of companion animals. Journal of the American Veterinary Medical Association 213(1):54-60.

Tizard, I. 1999. Grease, Anthraxgate, and kennel cough : a revisionist history of early veterinary vaccines. Advances in Veterinary medicine 41:7-24.

Trilateral seal expert meeting 06.06.2002. http://cwss.www.de/news/news/Seals/Reports/TrilateralSealMeeting.pdf

Twark, L., Dodds, W.J. 2000. Clinical use of serum parvovirus and distemper virus antibody titres for determining revaccination strategies in healthy dogs. Journal of the American veterinary Medical Association 217(7):1021-4.

Visee, A.M., Zwart, P., Haagsma, J. 1974. Two saces of infectious enteritis in maned wolves (Chrysocyon brachyurus ). Verhandlungsbericht XVI Internationalen Symposiums Ueber Erkrankungen Zootiere, Erfurt. Berlin: Akademie Verlag :67-69.

Visee, A. 2001. Distemper, Rabies and Parvovirus vaccination in a captive-breeding programme for the African wild dog (Lycaon pictus) in Northern Tanzania. Proceedings Erkrankungen der zootiere 40:243-250.

Visser, I.K.G., Vedder, E.J., Bildt van de, M.W., Groen, J., Orvell, C., Raga, J.A., Osterhaus, A.D.M.E. 1992. Canine distemper virus ISCOMs induce protection in harbour seals against phocid distemper but still allow subsequent infection with phocid distemper virus-1. Vaccine 10(7):435-438.

Vries de, P., UytdeHaag, F.G., Osterhaus, A.D.M.E. 1988. Canine distemper virus (CDV) immune stimulating complexes (ISCOMS), but not measles virus ISCOMS protect dogs against CDV infection. Journal of General Virology 69(8):2071-2083.

Wack, R.F., Kramer, L.W., Cupps, W.L., Katz, S. 1990. Antibody titre response of cheetah (acinnyx jubatus ) cubs to vaccination. Proceedings Of the American Association of Zoo Veterinarians Annual Conference: 147-149.

Wack, R.F. 1991. the vaccination of cheetahs ( acinonyx jubatus ). Proceedings of the American Association of Zoo Veterinarians Annual Conference:294-7.

Wack RF et al 1993. The response of cheetahs to routine vaccination. Journal of Zoo and Wildlife Medicine 109-117.

VI. Vaccination of Non-Domestic Carnivores : a Review

Whetstone, C.A., Draayer, H., Collins, J.E. 1988. Characterization of canine adenovirus type 1 isolated from American black bears. American Journal of Veterinary Research 49(6):778- 80.

Whetstone, C.A., Bunn, T.O., Emmons, R.W., Wiktor, T.J. 1984. Use of monoclonal antibodies to confirm vaccine-induced rabies in ten dogs two cats and one Fox. Journal of the American Veterinary Medical Association 185(3):285-8.

Williams, E.S., Anderson, S.L., Cavender, J., list, K., Heam, C., Appel, M.J.G. 1996. Vaccination of black-footed ferret ( mustela nigripes ) x siberian polecat ( mustela eversmann ) hybrids and domestic ferrets ( mustela putorius furo ) against canine distemper. Journal of Wildlife Diseases 32(3):417-423.

Williams ES, Montali RJ, 1998. Vaccination of black-footed ferret x siberian polecat hybrids against canine distemper with recombinant and modified live virus vaccines. Proceedings of the Annual Conference of the Wildlife Disease Association 1998:107.

Williams, E.S., Thorne, E.T. 1999. Veterinary contribution to the black-footed ferret conservation programme. In: Fowler, M.E. & Miller, R.E.: Zoo and wild animal medicine, Current therapy 4 . Saunders Co: 460-463.

Wilson, R.B., Kord, C.E., Holladay, J.A. 1986. A neurologic syndrome associated with use of a canine coronavirus-parvovirus vaccine in dogs. Compendium on Continuing Education for the Practicing Veterinarian 8:117-124.

Wimsatt, J., Biggins, D., Taylor, B., Innes, K., Garell, D. 1999 Preliminary experimental canarypox vectored recombinant canine distemper vaccine evaluation in the siberian polecat (Mustela eversmanni ). Proceedings of the American Association of Zoo Veterinarians Annual Conference:351-352.

Wimsatt, J. Jay, M.T., Innes, K.E., Jessen, M., Collins, J.K. 2001. Serologic evaluation, efficacy, and safety of a commercial modified-live canine distemper vaccine in domestic ferrets. American Journal of Veterinary Reasearch 62(5):736-740.

Wimsatt, J., Biggins, D., Innes, K., Taylor, B., Garell, D. 2003. Evaluation of oral and subcutaneous delivery of an experimental canarypox recombinant canine distemper vaccine in the Siberian polecat ( Mustela eversmanni ). Journal of Zoo Wildlife Medicine 34(1):25-35.

Wood, S.L. et al 1995. Canine distemper virus-like infection in a captive African lioness . Canadian Veterinary Journal 36:34-35.

Woodford, M.H. (ed), 2001. Quarantine and health screening protocols for wildlife prior to translocation and release into the wild. Published jointly by the IUCN Species Survival Commission’s Veterinary Specialist Group, Gland, Switzerland, the Office International des Epizooties (OIE), Care for the Wild, UK, and the European Association of Zoo and Wildlife Veterinartians, Switzerland: 39-44.

Woolf, A., Swart, J. 1974. An outbreak of feline panleukopenia. Journal of Zoo Animal Medicine 5:32.